Open Access This article is
- freely available
Forests 2018, 9(6), 353; doi:10.3390/f9060353
Forest Regeneration Following Emerald Ash Borer (Agrilus planipennis Fairemaire) Enhances Mesophication in Eastern Hardwood Forests
Department of Biology, University of Findlay, 1000 North Main Street, Findlay, OH 45840 USA
Biology Department, Washington & Jefferson College, 60 South Lincoln Street, Washington, PA 15301 USA
Author to whom correspondence should be addressed.
Received: 9 March 2018 / Accepted: 10 May 2018 / Published: 14 June 2018
Emerald ash borer (EAB, Agrilus planipennis Fairemaire) is a phloem-feeding beetle that was introduced into North America in the late 20th century and is causing widespread mortality of native ash (Fraxinus) species. The loss of an entire genus from the forest flora is a substantial disturbance, but effects vary because of differences in Fraxinus dominance and remaining vegetation. At three sites near the center of the North American EAB range, we investigated the impacts of Fraxinus mortality on recruitment of woody and non-native vegetation in 14 permanent plots from 2012 to 2017. We used the change in relative Fraxinus basal area to determine the impact of EAB on density of woody species and non-native vegetation less than 2.5 cm diameter at breast height (dbh). Changes in canopy cover were not correlated with loss of Fraxinus from the overstory, and only the density of shade-tolerant shrubs and saplings increased with Fraxinus mortality. Both native and non-native shrub species increased in density at sites where they were present before EAB, but no new invasions were detected following Fraxinus mortality. These shifts in understory vegetation indicate that Fraxinus mortality enhances the rate of succession to shade-tolerant species.
Keywords:Fraxinus; Agrilus planipennis Fairemaire; mesophication; forest regeneration; disturbance
In the nearly two decades since emerald ash borer (EAB, Agrilus planipennis Fairemaire) was first detected in North America , the response has evolved from preventing or mitigating damage to Fraxinus [2,3,4] to understanding how the introduced insect might impact other species and ecosystem function in forest communities [5,6,7]. Forest plant communities of eastern North America, like any system, are dynamic and subject to change, and EAB’s impact on Fraxinus is not exceptional. By inducing Fraxinus mortality, EAB immediately reduces forest stand basal area and releases resources, which subsequently become available to other species [8,9,10].
As a component of mesophytic forests of eastern North America, particularly those within Eastern US Lowland Forest Region—Upland Forest Types , Fraxinus species might well be considered a minor component of the system, represented primarily by F. americana L. and F. pennsylvanica Marshall . But these species have a wide distribution, and despite their relatively low abundance in this forest type , the loss of Fraxinus by EAB has the potential to drive changes in plant communities throughout the region, similar in respect to previous introductions that changed forest composition on a broad scale. Chestnut blight (Cryphonectria parasitica (Murrill) Barr) led to the widespread loss of Castanea dentata (Marshall) Borkh. throughout its native North American range, particularly in the Appalachian region , and Dutch elm disease (Ophiostoma ulmi Buisman (Melin and Nannf.), O. novo-ulmi Brasier) reduced Ulmus species to minor understory tree species in mesophytic forests across the continent . More recently, the exotic insects hemlock woolly adelgid (Adelges tsugae Annand) and beech scale (Cryptococcus fagisuga Lindinger) are influencing the structure and composition of eastern North American forests . In all instances, the change in canopy structure associated with the loss of individual trees has been marked by a shift to increasing dominance of shade-tolerant species in the understory and overstory layers [15,16,17,18,19,20].
Because the loss of Fraxinus from the canopy is similar to that of these species, we might expect similar responses in the understory. Indeed, in regard to changes already described in Ohio and Michigan, where EAB was initially detected and where Fraxinus is a relatively important component of the forest ecosystem, the loss of Fraxinus from the canopy induced growth of intermediate canopy trees, especially shade-tolerant Acer and Ulmus . Trees from these genera existed in the canopy prior to EAB and were better able to utilize resources in EAB-induced gaps than trees from other genera, including Quercus and Carya [8,21,22,23]. Even in wetter sites, preinvasion surveys indicate that co-dominant shade-tolerant trees are predicted to replace F. nigra (Marshall) in Ohio, Michigan, and Minnesota [24,25,26].
This pattern of change after pest-induced canopy loss generally follows predicted plant community succession from shade-intolerant and intermediate-tolerant species to dominance by shade-tolerant species. This continued process of transition in eastern North American forests has been termed “mesophication” , and these changes in canopy composition come with cascade effects and positive feedback on ecosystems, including changes to flammability, soil moisture, nutrient dynamics, decomposition, and forest regeneration [28,29,30]. EAB-induced Fraxinus mortality is likely hastening the process.
Since Fraxinus received scant attention prior to EAB, little is known about the long-term response of woody species at the ground level to the release of resources following the loss of Fraxinus trees. Initial descriptions of the seedling layer in EAB-impacted forests primarily show shade-tolerant species, including Acer rubrum L., A. saccharum Marshall., Ulmus americana L., Prunus serotina Ehrh., and Quercus rubra L. [9,23,24,31], but evidence of their persistence over time is lacking, and interactions between native woody seedlings and exotic invasive plants may further influence the composition of forests. Recent evidence suggests that existing invasive plants will increase in size following the release of resources by EAB-induced Fraxinus mortality .
We seek to understand the changes in richness and abundance of woody species, including their invasive competitors, in the years following EAB invasion. Specifically, we examine forest regeneration at the seedling and sapling layers, including the recruitment of seedlings into the sapling layer over a 5-year period following infestation. In addition, we are investigating shifts in the abundance of woody invasive species, especially those that compete with woody seedlings and saplings and have the potential to alter successional trajectories. We hypothesize that EAB indirectly increases the prevalence of shade-tolerant species in the understory, thus enhancing the process of mesophication.
2. Materials and Methods
2.1. Study Sites
Our 4 study sites are located in the deciduous forests of eastern North America and are associated with 3 colleges and universities: Baldwin-Wallace University (BW; Ohio), University of Findlay (UF; Ohio), and Washington & Jefferson College (WJ; Pennsylvania; Figure 1). All sites contain Fraxinus spp. but are generally dominated by other deciduous tree species (Table 1). Total basal area by plot ranges from 18 to 54 m2∙ha−1, including substantial differences in relative contributions of Fraxinus (Figure 2). Year of EAB detection was determined by decline of the Fraxinus canopy and confirmed by the presence of EAB exit holes. Only 1 site at UF is located in a floodplain; the rest are upland sites. Across these 4 sites, mean growing season length varies from 159 to 173 days, mean precipitation varies from 847 to 1132 mm, and mean annual temperature varies from 9.6 to 11.8 °C (Table 1). Soils are predominantly finer textured, from silty loam to silty clay loam .
2.2. Data Collection
We used the existing infrastructure of the Permanent Forest Plot Project (PFPP), one of the projects associated with the Ecological Research as Education Network (EREN; http://erenweb.org/). This project was launched in 2012 to establish a set of permanent research plots to address questions related to tree biomass, carbon accumulation, invasive species, and disturbance patterns across a range of sites and ecoregions . Participants establish at least 1 permanent 400-m2 plot in a forested area, identify and measure the diameter of all trees (>2.5 cm diameter at breast height (dbh), or 1.37 m above the ground), identify and tally all saplings (0–2.5 cm dbh, but at least 1.37 m tall) in 3 randomly selected subplots (25 m2), and characterize their site and plot using a standard protocol . PFPP data are entered in a secure online database accessible to all PFPP participants.
We also scaffolded 4 variables onto PFPP to evaluate the impact of EAB on Fraxinus trees. Tree damage indicates whether the tree is broken, uprooted, or leaned on by another tree (including Fraxinus); this variable was incorporated into the PFPP protocol . Ash rating  and ash tree breakup  indicate the level of decline, mortality, and breaking down of Fraxinus trees. We also counted the number of EAB exit holes observed between 1.25 and 1.75 m above the ground as a physical indicator that EAB is associated with the Fraxinus decline. These 3 variables are specific to the EAB Impacts Study , another EREN project.
To address questions related to the successional dynamics of forests, we built variables to characterize the understory plant community in the Complementary Vegetation (cVeg) Survey . Canopy cover was measured using a concave spherical densiometer (Model C, Robert E. Lemmon, Rapid City, SD, USA), while all woody plants between 0.3 and 1.37 m tall (i.e., shrubs and saplings) were identified and tallied within each of the three 25-m2 subplots used in the PFPP. In addition, all woody seedlings (<0.3 m tall) and non-woody plants were identified and tallied within 1-m2 miniplots in each of the subplots. Woody species were classified according to their shade tolerance [39,40].
For our study, we used 2 plots from Rocky River (BW; 2016–2017), 2 plots from the Olive Street site (UF; 2012, 2014–2017), 4 plots from the Rieck Center (UF; 2012, 2014–2017), and 6 plots from Abernathy Field Station (AFS, WJ; 2012, 2014–2017). All of the PFPP, EAB, and cVeg variables were measured at each of the sampling years by site.
Given our hypothesis that the loss of Fraxinus is driving a shift in community composition toward more mesophytic, or shade-tolerant, species, as well as increasing the prevalence of invasive plant species, we used the preinvasion relative basal area of Fraxinus as the independent variable. This variable was calculated as the proportion of cumulative basal area (BA = π × (0.5 × dbh)2) of 3 Fraxinus species (F. americana, F. pennsylvanica, F. quadrangulata Michx.) relative to all other trees prior to (BW and WJ sites) or at (UF sites) the time of EAB detection. The variables of interest, such as annual changes in woody seedling density, invasive plant density, and sapling and shrub density, partitioned by shade tolerance [39,40], were calculated as the annual change in density from the first to last sampling year and divided by the number of years of sampling, whether we had 2 (BW) or 5 (UF, WJ) years of data. Data from miniplots (woody seedling and forb) and subplots (shrubs and saplings) were pooled by plot, thus plot became the observational unit. Each of these dependent variables was then linearly regressed onto the relative basal area of Fraxinus. All analyses were conducted using IBM SPSS Statistics v.24 (IBM Corp., North Castle, NY, USA).
To determine whether we could detect changes in light resources at the forest floor, we regressed change in canopy cover on relative Fraxinus basal area prior to EAB invasion. Across all four sites, we found no significant relationship between canopy cover and relative Fraxinus dominance (p = 0.46), thus no evidence that light resources increased more in sites with greater dominance of Fraxinus (Figure 3).
The relative basal area of Fraxinus has not significantly affected the density of woody seedlings across sites (p > 0.18), whether with combined species or when partitioned by shade tolerance (Figure 4), yet some patterns are emerging. For example, shade-tolerant species increased in density at a higher rate in sites with more Fraxinus trees. Seedling density for F. americana generally declined across all sites, yet F. pennsylvanica seedlings generally increased in density at both UF sites (in supplementary file Table S1). Across UF and WJ sites, the density of Parthenocissus quinquefolia (L.) Planch. seedlings increased since EAB invasion. Other species, including the non-native Rosa multiflora Thunb. experienced both increased and decreased density within sites (Table S1).
While total shrub density (Figure 5a), including shade-intolerant species (Figure 5c), did not respond to changes in relative basal area of Fraxinus, shade-tolerant shrubs significantly (p = 0.005) increased in density (Figure 5b). This response appears to be driven by individual plots at the BW (Rocky-1) and UF (Olive-2) sites, both of which had higher losses of Fraxinus than other plots (Figure 2); two native shrubs, Lindera benzoin L. and Asimina triloba (L.) Dunal, respectively, substantially increased in these plots, but the non-native Rosa multiflora also increased in density over this same period at UF (Olive-2) (in supplementary file Table S2). Saplings of Fraxinus spp. generally increased at UF (Rieck) and WJ (AFS), as did the native Celtis occidentalis at UF (Rieck) and non-native Celastrus orbiculatus Thunb. and native Rubus spp. at WJ (AFS). However, Lindera benzoin generally decreased in density at WJ (AFS), while the non-native Lonicera spp. and Rosa multiflora Thunb. increased in the UF (Olive-1) plot that experienced widespread canopy tree loss from the June 2012 North American derecho (Table S2).
Relative basal area of Fraxinus was not a significant predictor of density of non-native vegetation in the ground layer or the shrub and sapling layer in 2017 (Figure 6). Only two plots, one each at WJ (AFS) and UF (Olive), saw above-average increases in non-native species density, yet both sites had relatively low relative amounts of Fraxinus basal area. And though three non-native species, Celastrus orbiculatus Thunb., Lonicera maackii (Rupr.) Maxim. and Rosa multiflora, increased in density in the shrub layer within sites during the period of study (Table S2), the overall change in non-native species density does not show a relationship to the decrease in relative Fraxinus basal area.
The loss of Fraxinus from mesophytic North American hardwood forests and the subsequent release of resources appear to have little influence on the distribution and abundance of forest regeneration at the seedling and sapling level. Furthermore, we found no evidence that this loss alters the process of mesophication in the same manner as acute, severe disturbances that typically impact canopy cover.
4.1. Canopy Cover
Light is the primary resource expected to change at the ground layer as a result of the death of large overstory Fraxinus trees , yet our evidence suggests that the protracted decline and ultimate death of Fraxinus individuals does not create conditions that substantially alter the light regime on the forest floor, as measured by our canopy cover index. Although canopy cover decreased at a rate of 0%–3% annually, there was no detectable relationship to Fraxinus mortality (Figure 3). In order to meet the physiological demands of shade-intolerant species, like Quercus and Carya, light levels need to reach 25%–50% full sunlight , which is often reached with more severe disturbances, like shelterwood harvesting .
Research on canopy trees in response to EAB-induced Fraxinus mortality shows that existing canopy trees respond positively. Gaps concurrently fill with non-Fraxinus species , likely influencing the lack of substantial change in annual canopy cover over time. Recent evidence using LIDAR (Light Detection and Ranging) indicates that single-tree death in northern hardwood forests is not sufficient to generate canopy gaps where the subcanopy is well developed , suggesting that the gradual canopy opening that occurs with EAB-induced Fraxinus mortality is less likely to enrich the ground layer with light than it is to promote the growth of existing subcanopy trees.
Indeed, in northwest Ohio, the relative growth rates of the shade-tolerant species Acer saccharum and Ulmus americana were faster than other species in the forest canopy following Fraxinus mortality , and smaller trees exhibited faster growth rates than larger ones, suggesting that subcanopy individuals benefit more than the co-dominant overstory trees. Trees remaining in the canopy of our forest sites include mesophytic species, typically from Acer, Prunus, Ulmus, and Celtis (Table 1), which supports our hypothesis that Fraxinus loss will increase the speed at which forests are dominated by more shade-tolerant species.
4.2. Understory Composition and Density
The composition of woody species in the seedling layer is relatively stable following the loss of Fraxinus to EAB. We detected no statistically significant relationship between the loss of Fraxinus and the change in seedling density (Figure 4). In regard to individual species, there is a large amount of variability among sites and plots. Species with the largest, most consistent increases over time include the native vine Parthenocissus quinquefolia, while the non-native shrub Rosa multiflora increased or decreased across sites, indicating a lack of relationship with Fraxinus loss. Interestingly, the number of Fraxinus seedlings increased at both UF (Olive) plots, where overstory Fraxinus trees had succumbed to EAB beginning in 2012 (Table S1). Recent evidence suggests that Fraxinus seedbanks do not persist beyond the life of the tree , indicating that an off-site seed source persists for this site.
The shrub and sapling layer was more responsive to Fraxinus mortality than the seedling layer. As the amount of Fraxinus basal area increased in plots, the density of shade-tolerant species increased (r2 = 0.50, p = 0.005). This was in contrast to the lack of association detected between Fraxinus basal area and the change in shade-intolerant species density (r2 = 0.003, p = 0.853). The increase in shade-tolerant species density coincides with evidence of established trees in the mid-canopy responding to the resources made available through the mortality of Fraxinus individuals. The response of individual species varied across sites, but those with increases at more than one site include shade-tolerant Lindera benzoin and Asimina triloba, both native understory species.
Our findings are not unusual, as shrub and sapling density has been shown to increase in response to species-specific canopy dieback elsewhere. In Europe, fungal-induced Fraxinus excelsior L. dieback promoted the growth of widely distributed shade-tolerant shrubs and understory trees, including Corylus avellana L., Prunus padus L., and Lonicera xylosterum L. . In North America, after Dutch elm disease induced Ulmus decline, the intermediate- and shade-tolerant shrubs Alnus rugosa (L.) Moench, Viburnum recognitum Fern., and Cornus stolonifera L. in wetland habitats responded more positively in gaps created by the death of Ulmus stems in the overstory than seedlings of other canopy trees . In southeastern Wisconsin, species composition and density of woody seedlings were not associated with density of dead Ulmus, yet the density of shrubs, especially Ribes spp., Rubus spp., and Cornus racemosa Lam., was associated with Ulmus mortality .
4.3. Invasive Species
No new invasive species were detected in the research plots. For plots with existing invasive plants, some became more numerous, including Lonicera maackii, Rosa multiflora, and Celastrus orbiculatus, but because of variability among plots, we were unable to identify Fraxinus mortality as the primary cause of the increase at our sites. Prior to EAB invasion, one plot at the UF (Olive) site had large numbers of L. maackii and R. multiflora; these species increased in density over time. This particular site, however, was also strongly influenced by a storm that caused significant loss of the overstory in 2012. The confounding disturbances of storm damage and EAB-induced Fraxinus mortality cannot be distinguished. Recent evidence suggests that the amount of Fraxinus, and thus the amount of light increasing beneath the canopy, influences the response of existing L. maackii; in a comprehensive study of population-level responses to EAB, existing L. maackii individuals had increased stem diameter following Fraxinus mortality, while the number of individual plants, amount of fruiting, and height of the shrubs were not impacted .
Additionally, in three plots in Pennsylvania, Celastrus orbiculatus had higher annual increases in density than other species following EAB, but because of losses to this species in other plots at the same site and an overall lack of relationship between Fraxinus basal area and shrub and sapling density (Figure 6b; r2 = 0.001, p = 0.955), the increase in this species was not likely caused by the loss of Fraxinus.
Our evidence shows that the resources released through Fraxinus mortality are insufficient to modify the process of mesophication in mesophytic forests, but instead generate changes that resemble those observed with small gaps. The primary beneficiaries of released resources include individuals already existing in the understory canopy, among them small shade-tolerant trees, saplings, and shrubs typical of mature mesophytic forests, conforming to what is observed in forest gap dynamics [8,49,50,51,52]. This enhanced mesophication resulting from the loss of Fraxinus has allowed shade-tolerant species, including those restricted to understory canopy positions, like Asimina triloba (L.) Dunal and Lindera benzoin L., to increase in the shrub and sapling layer at faster rates than shade-intolerant species (Figure 5). As mesophication has been noted throughout much of the eastern North American forest complex [28,53,54,55], we would expect to see similar patterns throughout the region where F. pennsylvanica and F. americana are the primary Fraxinus species represented in the canopy.
Importantly, some of our sites are in regions with relatively high amounts of Fraxinus compared to other mesophytic forest regions of eastern North America . Our research primarily includes sites with relative Fraxinus basal area within the range of 5–25%, and we find no compelling evidence that the loss of trees at our sites impacts regeneration and recruitment. Where Fraxinus is a smaller component of the forest tree community, we expect that, like our sites, these areas will not see dramatic shifts in seedling and shrub composition resulting from the loss of Fraxinus in the overstory.
With the exception of Fraxinus, EAB is not a disturbance that influences the abundance of woody species regeneration and subsequent recruitment in sites where Fraxinus is a minor component of the canopy vegetation. The five species of Fraxinus most common to eastern hardwood forests, F. americana, F. pennsylvanica, F. nigra, F. profunda Bush, and F. quadrangulata, have been classified as critically endangered and on the brink of extinction by the International Union for Conservation of Nature (IUCN) [56,57,58,59,60]. Conservation of the genus is important, but the consequence of losing the species has little influence on immediate future successional pathways of woody vegetation in the forests where Fraxinus is a minor component.
The following are available online at https://www.mdpi.com/1999-4907/9/6/353/s1: Table S1. Annual change in density (ha-1) of woody seedlings (<0.30 m tall) by plot after EAB invasion. Empty cells indicate species absence. Table S2. Annual change in density (ha–1) of shrubs and saplings (woody plants, 0.30–1.37 m tall) by plot after EAB invasion. Empty cells indicate species absence.
B.J.D. and J.S.K. developed the research questions, conceived the design for the EAB Impacts Study and Complementary Vegetation (cVeg) Survey, collected the data, performed the analyses, and wrote the manuscript. Both B.J.D. and J.S.K. provided edits and comments during the drafting of the paper.
This research received no external funding.
The Ecological Research as Education Network (EREN) was funded with the support of a Research Coordination Grant from the Research Coordination Network—Undergraduate Biology Education Program of the U.S. National Science Foundation (DEB 0955344, 2010–2016). We are grateful to our home institutions for funding and for supporting travel to work together, and we are thankful for the contributions of data, discussions, and analyses of changes in the invasive plant species by Kathryn Flinn (Baldwin-Wallace University). For access to field sites, we thank Cleveland Metroparks (Rocky River), University of Findlay (Olive Street, Rieck Center), and the Abernathy family (Abernathy Field Station). We appreciate the online site data gained from the PFPP database. We also thank the myriad undergraduate students and two high school students who contributed to data collection, and the reviewers who improved this manuscript with insightful comments and suggestions.
Conflicts of Interest
The authors declare no conflict of interest.
- Haack, R.A.; Jendak, E.; Houping, L.; Marchant, K.R.; Petrice, T.R.; Poland, T.M.; Ye, H. The emerald ash borer: A new exotic pest in North America. Newsl. Mich. Entomological Soc. 2002, 47, 1–5. [Google Scholar]
- Poland, T.M.; McCullough, D.G. Emerald Ash Borer: Invasion of the Urban Forest and the Threat to North America’s Ash Resource. J. For. 2006, 104, 118–124. [Google Scholar] [CrossRef]
- Animal and Plant Health Inspection Service, USDA. Emerald Ash Borer: Quarantine and Regulations. Available online: https://www.federalregister.gov/d/03-25881 (accessed on 15 April 2018).
- Herms, D.A.; McCullough, D.G. Emerald Ash Borer Invasion of North America: History, Biology, Ecology, Impacts, and Management. Annu. Rev. Entomol. 2014, 59, 13–30. [Google Scholar] [CrossRef] [PubMed]
- Perry, K.I.; Herms, D.A.; Klooster, W.S.; Smith, A.; Hartzler, D.M.; Coyle, D.R.; Gandhi, K.J.K. Downed Coarse Woody Debris Dynamics in Ash (Fraxinus spp.) Stands Invaded by Emerald Ash Borer (Agrilus planipennis Fairmaire). Forests 2018, 9, 191. [Google Scholar] [CrossRef]
- Ricketts, M.P.; Flower, C.E.; Knight, K.S.; Gonzalez-Meler, M.A. Evidence of Ash Tree (Fraxinus spp.) Specific Associations with Soil Bacterial Community Structure and Functional Capacity. Forests 2018, 9, 187. [Google Scholar] [CrossRef]
- Marché, J.D., II. The Green Menace: Emerald Ash Borer and the Invasive Species Problem; Oxford University Press: Oxford, UK, 2017; ISBN 978-0-19-066892-1. [Google Scholar]
- Flower, C.E.; Knight, K.S.; Gonzalez-Meler, M.A. Impacts of the emerald ash borer (Agrilus planipennis Fairmaire) induced ash (Fraxinus spp.) mortality on forest carbon cycling and successional dynamics in the eastern United States. Biol. Invasions 2013, 15, 931–944. [Google Scholar] [CrossRef]
- Hoven, B.M.; Gorchov, D.L.; Knight, K.S.; Peters, V.E. The effect of emerald ash borer-caused tree mortality on the invasive shrub Amur honeysuckle and their combined effects on tree and shrub seedlings. Biol. Invasions 2017, 19, 2813–2836. [Google Scholar] [CrossRef]
- McCullough, D.G.; Siegert, N.W. Estimating potential emerald ash borer (Coleoptera: Buprestidae) populations using ash inventory data. J. Econ. Entomol. 2007, 100, 1577–1586. [Google Scholar] [CrossRef] [PubMed]
- Vankat, J.L. A classification of the forest types of North America. Vegetatio 1990, 88, 53–66. [Google Scholar] [CrossRef]
- MacFarlane, D.W.; Meyer, S.P. Characteristics and distribution of potential ash tree hosts for emerald ash borer. For. Ecol. Manag. 2005, 213, 15–24. [Google Scholar] [CrossRef]
- Anagnostakis, S.L. Chestnut blight: The classical problem of an introduced pathogen. Mycologia 1987, 79, 23–37. [Google Scholar] [CrossRef]
- Karnosky, D.F. Dutch elm disease: A review of the history, environmental implications, control, and research needs. Environ. Conserv. 1979, 6, 311–322. [Google Scholar] [CrossRef]
- Morin, R.S.; Liebhold, A.M. Invasions by two non-native insects alter regional forest species composition and successional trajectories. For. Ecol. Manag. 2015, 341, 67–74. [Google Scholar] [CrossRef]
- Elliott, K.J.; Swank, W.T. Long-term changes in forest composition and diversity following early logging (1919–1923) and the decline of American chestnut (Castanea dentata). Plant Ecol. 2007, 197, 155–172. [Google Scholar] [CrossRef]
- Stephenson, S.L. Changes in a former chestnut-dominated forest after a half century of succession. Am. Midl. Nat. 1986, 116, 173–179. [Google Scholar] [CrossRef]
- Myers, B.R.; Walck, J.L.; Blum, K.E. Vegetation change in a former chestnut stand on the Cumberland Plateau of Tennessee during an 80-year period (1921–2000). Castanea 2004, 69, 81–91. [Google Scholar] [CrossRef]
- Barnes, B.V. Succession in deciduous swamp communities of southeastern Michigan formerly dominated by American elm. Can. J. Bot. 1976, 54, 19–24. [Google Scholar] [CrossRef]
- Parker, G.R.; Leopold, D.J. Replacement of Ulmus americana L. in a mature east-central Indiana woods. Bull. Torrey Bot. Club 1983, 110, 482. [Google Scholar] [CrossRef]
- Costilow, K.C.; Knight, K.S.; Flower, C.E. Disturbance severity and canopy position control the radial growth response of maple trees (Acer spp.) in forests of northwest Ohio impacted by emerald ash borer (Agrilus planipennis). Ann. For. Sci. 2017, 74, 10. [Google Scholar] [CrossRef]
- Burr, S.J.; McCullough, D.G. Condition of green ash (Fraxinus pennsylvanica) overstory and regeneration at three stages of the emerald ash borer invasion wave. Can. J. For. Res. 2014, 44, 768–776. [Google Scholar] [CrossRef]
- Kolka, R.K.; D’Amato, A.W.; Wagenbrenner, J.W.; Slesak, R.A.; Pypker, T.G.; Youngquist, M.B.; Grinde, A.R.; Palik, B.J. Review of ecosystem level impacts of emerald ash borer on black ash wetlands: What does the future hold? Forests 2018, 9, 179. [Google Scholar] [CrossRef]
- Iverson, L.; Knight, K.S.; Prasad, A.; Herms, D.A.; Matthews, S.; Peters, M.; Smith, A.; Hartzler, D.M.; Long, R.; Almendinger, J. Potential species replacements for black ash (Fraxinus nigra) at the confluence of two threats: Emerald ash borer and a changing climate. Ecosystems 2015, 19, 248–270. [Google Scholar] [CrossRef]
- Davis, J.C.; Shannon, J.P.; Bolton, N.W.; Kolka, R.K.; Pypker, T.G. Vegetation responses to simulated emerald ash borer infestation in Fraxinus nigra dominated wetlands of Upper Michigan, USA. Can. J. For. Res. 2017, 47, 319–330. [Google Scholar] [CrossRef]
- Looney, C.E.; D’Amato, A.W.; Palik, B.J.; Slesak, R.A. Canopy treatment influences growth of replacement tree species in Fraxinus nigra forests threatened by the emerald ash borer in Minnesota, USA. Can. J. For. Res. 2017, 47, 183–192. [Google Scholar] [CrossRef]
- Nowacki, G.J.; Abrams, M.D. The demise of fire and “mesophication” of forests in the eastern United States. Bioscience 2008, 58, 123–138. [Google Scholar] [CrossRef]
- Alexander, H.D.; Arthur, M.A. Implications of a predicted shift from upland oaks to red maple on forest hydrology and nutrient availability. Can. J. For. Res. 2010, 40, 716–726. [Google Scholar] [CrossRef]
- Alexander, H.D.; Arthur, M.A. Increasing red maple leaf litter alters decomposition rates and nitrogen cycling in historically oak-dominated forests of the eastern U.S. Ecosystems 2014, 17, 1371–1383. [Google Scholar] [CrossRef]
- Kreye, J.K.; Varner, J.M.; Hiers, J.K.; Mola, J. Toward a mechanism for eastern North American forest mesophication: Differential litter drying across 17 species. Ecol. Appl. 2013, 23, 1976–1986. [Google Scholar] [CrossRef] [PubMed]
- Tatina, R. Changes in Fagus grandifolia and Acer saccharum abundance in an old-growth, beech-maple forest at Warren Woods State Park, Berrien County, Michigan, USA. Castanea 2015, 80, 95–102. [Google Scholar] [CrossRef]
- Natural Resources Conservation Service, United States Department of Agriculture. Web Soil Survey. Available online: https://websoilsurvey.sc.egov.usda.gov/ (accessed on 7 July 2017).
- Initial County EAB Detections in North America 2017. Available online: https://www.aphis.usda.gov/plant_health/plant_pest_info/emerald_ash_b/downloads/MultiState.pdf (accessed on 11 February 2018).
- Kuers, K.; Lindquist, L. PFPP Protocols and Datasheets. Available online: http://erenweb.org/new-page/carbon-storage-project/permanent-plot-protocol/pfpp-protocol-files/ (accessed on 9 March 2018).
- Smith, A. Effects of community structure on forest susceptibility and response to the emerald ash borer invasion of the Huron River watershed in southeast Michigan. Master’s Thesis, The Ohio State University, Columbus, OH, USA, 2006. [Google Scholar]
- Knight, K.S.; Flash, B.P.; Kappler, R.H.; Throckmorton, J.A.; Grafton, B.; Flower, C.E. Monitoring Ash (Fraxinus spp.) Decline and Emerald Ash Borer (Agrilus planipennis) Symptoms in Infested Areas; General Technical Report NRS-139; U.S. Department of Agriculture, Forest Service, Northern Research Station: Newtown Square, PA, USA, 2014; p. 18.
- Dolan, B.J.; Kilgore, J.S. Emerald Ash Borer Project. Available online: http://erenweb.org/new-page/eab/ (accessed on 11 February 2018).
- Kilgore, J.S.; Dolan, B.J. Complementary Vegetation Survey (cVeg). Available online: http://erenweb.org/new-page/cveg/ (accessed on 11 February 2018).
- Baker, F.S. A revised tolerance table. J. For. 1949, 47, 179–181. [Google Scholar] [CrossRef]
- Niinemets, Ü.; Valladares, F. Tolerance to shade, drought, and waterlogging of temperate northern hemisphere trees and shrubs. Ecol. Monogr. 2006, 76, 521–547. [Google Scholar] [CrossRef]
- Canham, C.D.; Denslow, J.S.; Platt, W.J.; Runkle, J.R.; Spies, T.A.; White, P.S. Light regimes beneath closed canopies and tree-fall gaps in temperate and tropical forests. Can. J. For. Res. 1990, 20, 620–631. [Google Scholar] [CrossRef]
- Gottschalk, KW. Shade, leaf growth and crown development of Quercus rubra, Quercus velutina, Prunus serotina and Acer rubrum seedlings. Tree Physiol. 1994, 14, 735–749. [Google Scholar] [CrossRef] [PubMed]
- Parker, W.C.; Dey, D.C. Influence of overstory density on ecophysiology of red oak (Quercus rubra) and sugar maple (Acer saccharum) seedlings in central Ontario shelterwoods. Tree Physiol. 2008, 28, 797–804. [Google Scholar] [CrossRef] [PubMed]
- Senécal, J.-F.; Doyon, F.; Messier, C. Tree death not resulting in gap creation: An investigation of canopy dynamics of northern temperate deciduous forests. Remote Sens. 2018, 10, 17. [Google Scholar] [CrossRef]
- Klooster, W.S.; Herms, D.A.; Knight, K.S.; Herms, C.P.; McCullough, D.G.; Smith, A.; Gandhi, K.J.K.; Cardina, J. Ash (Fraxinus spp.) mortality, regeneration, and seed bank dynamics in mixed hardwood forests following invasion by emerald ash borer (Agrilus planipennis). Biol. Invasions 2014, 16, 859–873. [Google Scholar] [CrossRef]
- Pušpure, I.; Laiviņš, M.; Matisons, R.; Gaitnieks, T. Understory changes in Fraxinus excelsior stands in response to dieback in Latvia. Proc. Latv. Acad. Sci. 2016, 70, 131–137. [Google Scholar] [CrossRef]
- Huenneke, L.F. Understory response to gaps caused by the death of Ulmus americana in central New York. Bull. Torrey Bot. Club 1983, 110, 170–175. [Google Scholar] [CrossRef]
- Dunn, C.P. Shrub layer response to death of Ulmus americana in southeastern Wisconsin lowland forests. Bull. Torrey Bot. Club 1986, 113, 142. [Google Scholar] [CrossRef]
- Poulson, T.L.; Platt, W.J. Replacement patterns of beech and sugar maple in Warren Woods, Michigan. Ecology 1996, 77, 1234–1253. [Google Scholar] [CrossRef]
- Yamamoto, S.-I. The gap theory in forest dynamics. Bot. Mag. Tokyo 1992, 105, 375–383. [Google Scholar] [CrossRef]
- Hart, J.L.; Grissino-Mayer, H.D. Gap-scale disturbance processes in secondary hardwood stands on the Cumberland Plateau, Tennessee, USA. Plant Ecol. 2008, 201, 131–146. [Google Scholar] [CrossRef]
- Cowell, C.M.; Mark Cowell, C.; Hoalst-Pullen, N.; Jackson, M.T. The limited role of canopy gaps in the successional dynamics of a mature mixed Quercus forest remnant. J. Veg. Sci. 2010, 21, 201–212. [Google Scholar] [CrossRef]
- Flatley, W.T.; Lafon, C.W.; Grissino-Mayer, H.D.; LaForest, L.B. Changing fire regimes and old-growth forest succession along a topographic gradient in the Great Smoky Mountains. For. Ecol. Manage. 2015, 350, 96–106. [Google Scholar] [CrossRef]
- Chapman, J.I.; McEwan, R.W. Thirty years of compositional change in an old-growth temperate forest: The role of topographic gradients in oak-maple dynamics. PLoS ONE 2016, 11, e0160238. [Google Scholar] [CrossRef] [PubMed]
- Knopp, P.D. The distribution of Quercus rubra in the Maumee Lake Plain of southeastern Michigan. Am. Midl. Nat. 2012, 168, 70–92. [Google Scholar] [CrossRef]
- Jerome, D.; Westwood, M.; Oldfield, S.; Romero-Severson, J. Fraxinus Americana. Available online: http://www.iucnredlist.org/details/61918430/0 (accessed on 11 February 2018).
- Westwood, M.; Oldfield, S.; Jerome, D.; Romero-Severson, J. Fraxinus quadrangulata. Available online: http://www.iucnredlist.org/details/61919112/0 (accessed on 11 February 2018).
- Jerome, D.; Westwood, M.; Oldfield, S.; Romero-Severson, J. Fraxinus nigra. Available online: http://www.iucnredlist.org/details/61918683/0 (accessed on 11 February 2018).
- Westwood, M.; Oldfield, S.; Jerome, D.; Romero-Severson, J. Fraxinus pennsylvanica. Available online: http://www.iucnredlist.org/details/61918934/0 (accessed on 11 February 2018).
- Westwood, M.; Jerome, D.; Oldfield, S.; Romero-Severson, J. Fraxinus profunda. Available online: http://www.iucnredlist.org/details/61919022/0 (accessed on 11 February 2018).
Figure 1. Current distribution of Fraxinus spp. (shaded region) and emerald ash borer (EAB, Agrilus planipennis, hatched region) in North America. Study sites are indicated on the map: UF, University of Findlay, Findlay, Ohio; BW, Baldwin-Wallace University, Berea, Ohio; and WJ, Washington & Jefferson College, Washington, Pennsylvania. Known EAB distribution as of 1 December 2017 .
Figure 2. Cumulative basal area of trees by Fraxinus spp. (hatched) and non-Fraxinus (open) across plots at year of EAB detection at Baldwin-Wallace University (BW, 2015), University of Findlay (UF, 2010), and Washington & Jefferson College (WJ, 2012) sites.
Figure 3. Mean annual change in canopy cover as a function of relative basal area of Fraxinus spp. prior to EAB invasion across four sites (r2 = 0.048, p = 0.450). AFS: Abernathy Field Station.
Figure 4. Effects of relative Fraxinus basal area on change in density of (a) woody seedlings of all species (r2 = 0.04. p = 0.482), (b) shade-tolerant species (r2 = 0.14, p = 0.184), and (c) shade-intolerant species (r2 = 0.03, p = 0.526).
Figure 5. Effects of loss of Fraxinus on change in density of (a) shrubs and saplings of all species (r2 = 0.01, p = 0.764), (b) shade-tolerant species (r2 = 0.50, p = 0.005), and (c) shade-intolerant species (r2 = 0.003, p = 0.853).
Figure 6. Effects of relative Fraxinus basal area on density of non-native vegetation, including (a) woody seedlings and forbs in 2017 (r2 = 0.003, p = 0.843) and (b) shrubs and saplings (r2 = 0.001, p = 0.955) in 2017.
Table 1. Physical characteristics, dominant vegetation, and year of detected emerald ash borer (EAB) infestation by site. Mean growing season, annual precipitation, temperature, elevation, and predominant soil texture were determined following standard Permanent Forest Plot Project (PFPP) methods . MGS: mean growing season length; MAP: mean annual precipitation; MAT: mean annual temperature.
|Site||Institution||County||State||MGS (days)||MAP (mm)||MAT (°C)||Mean Elevation (m∙asl)||Predominant Soil Texture||Dominant Tree Species (in Order of Dominance)||Mean Plot Basal Area (m2∙ha−1)||Year of Detected EAB|
|Rocky River 41.411217° N, 81.881817° W||Baldwin-Wallace University (BW)||Cuyahoga||OH||173||1132||11.67||233||Silty loam||Fraxinus americana L., Ulmus rubra Muhl., Quercus rubra L., Carya glabra Miller, Acer saccharum Marshall||36.0||2012|
|Olive Street 41.002292° N, 83.642219° W||University of Findlay (UF)||Hancock||OH||159||847||10.81||240||Silty clay loam||Celtis occidentalis L., Acer saccharum, Fraxinus pennsylvanica Marshall, Carya cordiformis (Wangenh.) K.Koch, Juglans nigra L., Ulmus americana L.||25.7||2010|
|Rieck Center 40.950716° N, 83.549870° W||University of Findlay (UF)||Hancock||OH||159||857||10.81||250||Silty loam||Acer saccharum, Fraxinus pennsylvanica, Fagus grandifolia Ehrh., Ulmus americana||31.9||2010|
|Abernathy Field Station (AFS) 40.134110° N, 80.183625° W||Washington & Jefferson College (WJ)||Washington||PA||169||970||9.6||367||Silty loam||Prunus serotina Ehrh., Acer saccharum, Fraxinus americana, Carya ovata (Mill.) K.Koch||37.1||2014|
© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).